Participation of endotoxin in root canal infections: A systematic review and meta-analysis

Frederico Canato Martinho; Diego Guilherme Dias de Rabello; Luciana Louzada Ferreira; Gustavo Giacomelli Nascimento

doi:10.4103/ejd.ejd_84_17

European Journal of Dentistry, Table of Contents

Eur J Dent 2017; 11(03): 398-406
DOI: 10.4103/ejd.ejd_84_17

Review Article

Thieme Medical and Scientific Publishers Private Ltd. A-12, Second Floor, Sector -2, NOIDA -201301, India

Participation of endotoxin in root canal infections: A systematic review and meta-analysis

Authors

Frederico Canato Martinho

¹Department of Restorative Dentistry, São José dos Campos Dental School, State University of São Paulo, São Paulo
Diego Guilherme Dias de Rabello

¹Department of Restorative Dentistry, São José dos Campos Dental School, State University of São Paulo, São Paulo
Luciana Louzada Ferreira

¹Department of Restorative Dentistry, São José dos Campos Dental School, State University of São Paulo, São Paulo
Gustavo Giacomelli Nascimento

²Section of Periodontology, Department of Dentistry and Oral Health, Aarhus University, Aarhus, Denmark

Abstract

ABSTRACT

This systematic review and meta-analysis aimed to evaluate the relationship between endotoxin levels and presence of clinical signs/symptoms and radiographic features in patients with endodontic infection. Electronic searches were performed on Medline/PubMed, Embase, Cochrane Library, Scielo, Science Direct, Web of Knowledge and Scopus databases for identification of relevant studies published up to December 2016. Grey literature was searched in Google Scholar. The selected literature was reviewed independently by two authors. Clinical studies evaluating the levels of endotoxin and the presence of clinical and radiographic features were included in this review. In order to determine the relationship between endotoxin levels and presence of clinical signs/symptoms and radiographic features meta-analyses were performed. Among the 385 articles identified in the initial search, 30 were included for full-text appraisal and only eight studies met the inclusion criteria for this systematic review. Meta-analysis revealed that individuals having teeth with tenderness to percussion (TTP) (P = 0.04; I² 57%) and previous episode of pain (PEP) (P = 0.001; I² 81%) had higher levels of endotoxin than their counterparts. Size of radiographic lesion >2 mm (P = 0.02; I² 68%) and presence of root canal exudation (EX) (P = 0.0007; I² 0%) were associated with higher levels of endotoxin. This systematic review and meta-analyses provided a strong evidence that endotoxin are related with the presence of clinical signs/symptoms and radiographic features in patients with endodontic infection.

Key words:

Endodontic treatment - endotoxins - meta-analysis - systematic review

Full Text

References

REFERENCES
1 Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Antigenic activity of bacterial endodontic contents from primary root canal infection with periapical lesions against macrophage in the release of interleukin-1beta and tumor necrosis factor alpha. J Endod 2010; 36: 1467-74
2 Martinho FC, Chiesa WM, Zaia AA, Ferraz CC, Almeida JF, Souza-Filho FJ. et al. Comparison of endotoxin levels in previous studies on primary endodontic infections. J Endod 2011; 37: 163-7
3 Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Antigenicity of primary endodontic infection against macrophages by the levels of PGE(2) production. J Endod 2011; 37: 602-7
4 Martinho FC, Leite FR, Nascimento GG, Cirelli JA, Gomes BP. Clinical investigation of bacterial species and endotoxin in endodontic infection and evaluation of root canal content activity against macrophages by cytokine production. Clin Oral Investig 2014; 18: 2095-102
5 Marinho AC, Martinho FC, Leite FR, Nascimento GG, Gomes BP. Proinflammatory activity of primarily infected endodontic content against macrophages after different phases of the root canal therapy. J Endod 2015; 41: 817-23
6 Gomes BP, Lilley JD, Drucker DB. Associations of endodontic symptoms and signs with particular combinations of specific bacteria. Int Endod J 1996; 29: 69-75
7 Rôças IN, Siqueira Jr. JF. Identification of bacteria enduring endodontic treatment procedures by a combined reverse transcriptase-polymerase chain reaction and reverse-capture checkerboard approach. J Endod 2010; 36: 45-52
8 Rietschel ET, Brade H. Bacterial endotoxins. Sci Am 1992; 267: 54-61
9 Jacinto RC, Gomes BP, Shah HN, Ferraz CC, Zaia AA, Souza-Filho FJ. et al. Quantification of endotoxins in necrotic root canals from symptomatic and asymptomatic teeth. J Med Microbiol 2005; 54: 777-83
10 Vianna ME, Horz HP, Conrads G, Feres M, Gomes BP. Comparative analysis of endodontic pathogens using checkerboard hybridization in relation to culture. Oral Microbiol Immunol 2008; 23: 282-90
11 Endo MS, Martinho FC, Zaia AA, Ferraz CC, Almeida JF, Gomes BP. et al. Quantification of cultivable bacteria and endotoxin in post-treatment apical periodontitis before and after chemo-mechanical preparation. Eur J Clin Microbiol Infect Dis 2012; 31: 2575-83
12 Gomes BP, Endo MS, Martinho FC. Comparison of endotoxin levels found in primary and secondary endodontic infections. J Endod 2012; 38: 1082-6
13 Martinho FC, Gomes BP. Quantification of endotoxins and cultivable bacteria in root canal infection before and after chemomechanical preparation with 2.5% sodium hypochlorite. J Endod 2008; 34: 268-72
14 Gomes BP, Martinho FC, Vianna ME. Comparison of 2.5% sodium hypochlorite and 2% chlorhexidine gel on oral bacterial lipopolysaccharide reduction from primarily infected root canals. J Endod 2009; 35: 1350-3
15 Martinho FC, Chiesa WM, Marinho AC, Zaia AA, Ferraz CC, Almeida JF. et al. Clinical investigation of the efficacy of chemomechanical preparation with rotary nickel-titanium files for removal of endotoxin from primarily infected root canals. J Endod 2010; 36: 1766-9
16 Xavier AC, Martinho FC, Chung A, Oliveira LD, Jorge AO, Valera MC. et al. One-visit versus two-visit root canal treatment: Effectiveness in the removal of endotoxins and cultivable bacteria. J Endod 2013; 39: 959-64
17 Martinho FC, Gomes AP, Fernandes AM, Ferreira NS, Endo MS, Freitas LF. et al. Clinical comparison of the effectiveness of single-file reciprocating systems and rotary systems for removal of endotoxins and cultivable bacteria from primarily infected root canals. J Endod 2014; 40: 625-9
18 Cardoso FG, Ferreira NS, Martinho FC, Nascimento GG, Manhães Jr. LR, Rocco MA. et al. Correlation between volume of apical periodontitis determined by cone-beam computed tomography analysis and endotoxin levels found in primary root canal infection. J Endod 2015; 41: 1015-9
19 Schein B, Schilder H. Endotoxin content in endodontically involved teeth. J Endod 1975; 1: 19-21
20 Horiba N, Maekawa Y, Abe Y, Ito M, Matsumoto T, Nakamura H. et al. Correlations between endotoxin and clinical symptoms or radiolucent areas in infected root canals. Oral Surg Oral Med Oral Pathol 1991; 71: 492-5
21 Oliveira LD, Carvalho CA, Carvalho AS, Alves Jde S, Valera MC, Jorge AO. et al. Efficacy of endodontic treatment for endotoxin reduction in primarily infected root canals and evaluation of cytotoxic effects. J Endod 2012; 38: 1053-7
22 Vianna ME, Horz HP, Conrads G, Zaia AA, Souza-Filho FJ, Gomes BP. et al. Effect of root canal procedures on endotoxins and endodontic pathogens. Oral Microbiol Immunol 2007; 22: 411-8
23 Morrison DC, Kline LF. Activation of the classical and properdin pathways of complement by bacterial lipopolysaccharides (LPS). J Immunol 1977; 118: 362-8
24 Seltzer S, Farber PA. Microbiologic factors in endodontology. Oral Surg Oral Med Oral Pathol 1994; 78: 634-45
25 Ferraz CC, Henry MA, Hargreaves KM, Diogenes A. Lipopolysaccharide from Porphyromonas gingivalis sensitizes capsaicin-sensitive nociceptors. J Endod 2011; 37: 45-8
26 Diogenes A, Ferraz CC, Akopian AN, Henry MA, Hargreaves KM. LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons. J Dent Res 2011; 90: 759-64
27 Khan AA, Diogenes A, Jeske NA, Henry MA, Akopian A, Hargreaves KM. et al. Tumor necrosis factor alpha enhances the sensitivity of rat trigeminal neurons to capsaicin. Neuroscience 2008; 155: 503-9
28 Norton LA, Proffit WR, Moore RR. In vitro bone growth inhibition in the presence of histamine and endotoxins. J Periodontol 1970; 41: 153-7
29 Bandow K, Maeda A, Kakimoto K, Kusuyama J, Shamoto M, Ohnishi T. et al. Molecular mechanisms of the inhibitory effect of lipopolysaccharide (LPS) on osteoblast differentiation. Biochem Biophys Res Commun 2010; 402: 755-61
30 Hong CY, Lin SK, Kok SH, Cheng SJ, Lee MS, Wang TM. et al. The role of lipopolysaccharide in infectious bone resorption of periapical lesion. J Oral Pathol Med 2004; 33: 162-9
31 Kassem A, Henning P, Lundberg P, Souza PP, Lindholm C, Lerner UH. et al. Porphyromonas gingivalis stimulates bone resorption by enhancing RANKL (Receptor activator of NF-κB ligand) through activation of toll-like receptor 2 in osteoblasts. J Biol Chem 2015; 290: 20147-58
32 Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Correlation between clinical/radiographic features and inflammatory cytokine networks produced by macrophages stimulated with endodontic content. J Endod 2012; 38: 740-5
33 Martinho FC, Leite FR, Nóbrega LM, Endo MS, Nascimento GG, Darveau RP. et al. Comparison of Fusobacterium nucleatum and Porphyromonas gingivalis lipopolysaccharides clinically isolated from root canal infection in the induction of pro-inflammatory cytokines secretion. Braz Dent J 2016; 27: 202-7
34 The Joanna Briggs Institute. Joanna Briggs Institute Reviewers' Manual: Edition. Adelaide, Australia: Joanna Briggs Institute; 2013
35 DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7: 177-88
36 Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005; 5: 13
37 Hurley JC. Endotoxemia: Methods of detection and clinical correlates. Clin Microbiol Rev 1995; 8: 268-92
38 American Association of Endodontists. Glossary of Endodontic Terms. 9th ed.. Chicago, IL-USA: 2013
39 Zero DT, Zandona AF, Vail MM, Spolnik KJ. Dental caries and pulpal disease. Dent Clin North Am 2011; 55: 29-46
40 Owatz CB, Khan AA, Schindler WG, Schwartz SA, Keiser K, Hargreaves KM. et al. The incidence of mechanical allodynia in patients with irreversible pulpitis. J Endod 2007; 33: 552-6
41 Cahill CM, Dray A, Coderre TJ. Priming enhances endotoxin-induced thermal hyperalgesia and mechanical allodynia in rats. Brain Res 1998; 808: 13-22
42 Takayama S, Miki Y, Shimauchi H, Okada H. Relationship between prostaglandin E2 concentrations in periapical exudates from root canals and clinical findings of periapical periodontitis. J Endod 1996; 22: 677-80
43 McNicholas S, Torabinejad M, Blankenship J, Bakland L. The concentration of prostaglandin E2 in human periradicular lesions. J Endod 1991; 17: 97-100
44 Lim GC, Torabinejad M, Kettering J, Linkhardt TA, Finkelman RD. Interleukin 1-beta in symptomatic and asymptomatic human periradicular lesions. J Endod 1994; 20: 225-7
45 Kuo ML, Lamster IB, Hasselgren G. Host mediators in endodontic exudates. I. Indicators of inflammation and humoral immunity. J Endod 1998; 24: 598-603
46 Richards D, Rutherford RB. The effects of interleukin 1 on collagenolytic activity and prostaglandin-E secretion by human periodontal-ligament and gingival fibroblast. Arch Oral Biol 1988; 33: 237-43
47 Cohen JS, Reader A, Fertel R, Beck M, Meyers WJ. A radioimmunoassay determination of the concentrations of prostaglandins E2 and F2alpha in painful and asymptomatic human dental pulps. J Endod 1985; 11: 330-5
48 Garrison SW, Holt SC, Nichols FC. Lipopolysaccharide-stimulated PGE2 release from human monocytes. Comparison of lipopolysaccharides prepared from suspected periodontal pathogens. J Periodontol 1988; 59: 684-7
49 Offenbacher S, Heasman PA, Collins JG. Modulation of host PGE2 secretion as a determinant of periodontal disease expression. J Periodontol 1993; 64: 432-44
50 Horiba N, Maekawa Y, Abe Y, Ito M, Matsumoto T, Nakamura H. et al. Cytotoxicity against various cell lines of lipopolysaccharides purified from Bacteroides, Fusobacterium, and Veillonella isolated from infected root canals. J Endod 1989; 15: 530-4
51 Safavi KE, Rossomando EF. Tumor necrosis factor identified in periapical tissue exudates of teeth with apical periodontitis. J Endod 1991; 17: 12-4
52 Matsuo T, Ebisu S, Nakanishi T, Yonemura K, Harada Y, Okada H. et al. Interleukin-1 alpha and interleukin-1 beta periapical exudates of infected root canals: Correlations with the clinical findings of the involved teeth. J Endod 1994; 20: 432-5
53 Ataoğlu T, Ungör M, Serpek B, Haliloğlu S, Ataoğlu H, Ari H. et al. Interleukin-1beta and tumour necrosis factor-alpha levels in periapical exudates. Int Endod J 2002; 35: 181-5
54 Morishima M, Tanaka T, Takei M. Detections of endotoxin and microorganisms from root canals (author's transl). Aichi Gakuin Daigaku Shigakkai Shi 1980; 18: 88-93
55 Dahlén G, Bergenholtz G. Endotoxic activity in teeth with necrotic pulps. J Dent Res 1980; 59: 1033-40
56 Mattison GD, Haddix JE, Kehoe JC, Progulske-Fox A. The effect of Eikenella corrodens endotoxin on periapical bone. J Endod 1987; 13: 559-65
57 Yamasaki M, Nakane A, Kumazawa M, Hashioka K, Horiba N, Nakamura H. et al. Endotoxin and gram-negative bacteria in the rat periapical lesions. J Endod 1992; 18: 501-4
58 Delaissé JM, Eeckhout Y, Neff L, François-Gillet C, Henriet P, Su Y. et al. (Pro) collagenase (matrix metalloproteinase-1) is present in rodent osteoclasts and in the underlying bone-resorbing compartment. J Cell Sci 1993; 106 (04) 1071-82
59 Fuller K, Chambers TJ. Localisation of mRNA for collagenase in osteocytic, bone surface and chondrocytic cells but not osteoclasts. J Cell Sci 1995; 108 (06) 2221-30
60 Holliday LS, Welgus HG, Fliszar CJ, Veith GM, Jeffrey JJ, Gluck SL. et al. Initiation of osteoclast bone resorption by interstitial collagenase. J Biol Chem 1997; 272: 22053-8
61 Lin SK, Chiang CP, Hong CY, Lin CP, Lan WH, Hsieh CC. et al. Immunolocalization of interstitial collagenase (MMP-1) and tissue inhibitor of metalloproteinases-1 (TIMP-1) in radicular cysts. J Oral Pathol Med 1997; 26: 458-63
62 Lin SK, Kok SH, Kuo MY, Wang TJ, Wang JT, Yeh FT. et al. Sequential expressions of MMP-1, TIMP-1, IL-6, and COX-2 genes in induced periapical lesions in rats. Eur J Oral Sci 2002; 110: 246-53
63 Lin SK, Kok SH, Lin LD, Wang CC, Kuo MY, Lin CT. et al. Nitric oxide promotes the progression of periapical lesion via inducing macrophage and osteoblast apoptosis. Oral Microbiol Immunol 2007; 22: 24-9
64 Lin SK, Kok SH, Kuo MY, Lee MS, Wang CC, Lan WH. et al. Nitric oxide promotes infectious bone resorption by enhancing cytokine-stimulated interstitial collagenase synthesis in osteoblasts. J Bone Miner Res 2003; 18: 39-46
65 Tang Y, Sun F, Li X, Zhou Y, Yin S, Zhou X. et al. Porphyromonas endodontalis lipopolysaccharides induce RANKL by mouse osteoblast in a way different from that of Escherichia coli lipopolysaccharide. J Endod 2011; 37: 1653-8
66 Lin J, Bi L, Yu X, Kawai T, Taubman MA, Shen B. et al. Porphyromonas gingivalis exacerbates ligature-induced, RANKL-dependent alveolar bone resorption via differential regulation of toll-like receptor 2 (TLR2) and TLR4. Infect Immun 2014; 82: 4127-34
67 Haffajee AD, Socransky SS, Dibart S, Kent Jr. RL. Response to periodontal therapy in patients with high or low levels of P. gingivalis, P. intermedia, P. nigrescens and B. forsythus . J Clin Periodontol 1996; 23: 336-45
68 Dixon DR, Reife RA, Cebra JJ, Darveau RP. Commensal bacteria influence innate status within gingival tissues: A pilot study. J Periodontol 2004; 75: 1486-92
69 Darveau RP, Pham TT, Lemley K, Reife RA, Bainbridge BW, Coats SR. et al. Porphyromonas gingivalis lipopolysaccharide contains multiple lipid A species that functionally interact with both toll-like receptors 2 and 4. Infect Immun 2004; 72: 5041-51
70 Al-Qutub MN, Braham PH, Karimi-Naser LM, Liu X, Genco CA, Darveau RP. et al. Hemin-dependent modulation of the lipid A structure of Porphyromonas gingivalis lipopolysaccharide. Infect Immun 2006; 74: 4474-85
71 Herath TD, Darveau RP, Seneviratne CJ, Wang CY, Wang Y, Jin L. et al. Tetra- and penta-acylated lipid A structures of Porphyromonas gingivalis LPS differentially activate TLR4-mediated NF-κB signal transduction cascade and immuno-inflammatory response in human gingival fibroblasts. PLoS One 2013; 8: e58496-85
72 Galanos C, Lüderitz O, Rietschel ET, Westphal O, Brade H, Brade L. et al. Synthetic and natural Escherichia coli free lipid A express identical endotoxic activities. Eur J Biochem 1985; 148: 1-5
73 Curtis MA, Percival RS, Devine D, Darveau RP, Coats SR, Rangarajan M. et al. Temperature-dependent modulation of Porphyromonas gingivalis lipid A structure and interaction with the innate host defenses. Infect Immun 2011; 79: 1187-93